New soft tissue data of pterosaur tail vane reveals sophisticated, dynamic tensioning usage and expands its evolutionary origins.

Pterosaurs were the first vertebrates to achieve powered flight. Early pterosaurs had long stiff tails with a mobile base that could shift their center of mass, potentially benefiting flight control. These tails ended in a tall, thin soft tissue vane that would compromise aerodynamic control and efficiency if it fluttered during flight like a flag in the wind. Maintaining stiffness in the vane would have been crucial in early pterosaur flight, but how this was achieved has been unclear, especially since vanes were lost in later pterosaurs and are absent in birds and bats. Here we use Laser-Stimulated Fluorescence imaging to reveal a cross-linking lattice within the tail vanes of early pterosaurs. The lattice supported a sophisticated dynamic tensioning system used to maintain vane stiffness, allowing the whole tail to augment flight control and the vane to function as a display structure.

Intraspecific variation in the pterosaur Rhamphorhynchus muensteri-implications for flight and socio-sexual signaling.

Pterosaurs were the first powered flying vertebrates, with a fossil record that stretches back to about 230 million years before present. Most species are only known from one to three specimens, which are most often fragmentary. However, Rhamphorhynchus muensteri is known from numerous excellent specimens, including multiple specimens with soft tissue preservation. As such, Rhamphorhynchus muensteri is one of the only pterosaurs amenable to analysis for intraspecific variation. It has been previously predicted that elements directly involved in the flight apparatus, such as those of the forelimb, will be more highly constrained in their proportions than other parts of the skeleton. We investigated the degree of variation seen in elements and body parts of Rhamphorhynchus, which represents the best model system among pterosaurs for testing these expectations of intraspecific variation. We recover evidence for high levels of constraint throughout the appendicular and axial elements (head, neck, torso, tail, forelimbs, hindlimbs), suggesting that all were important for flight. We further find that tail variation increases among the largest specimens, suggesting reduced constraint and/or stronger sexual selection on the tail in more mature individuals.

The Role of Locomotory Ancestry on Secondarily Aquatic Transitions.

Land-to-sea evolutionary transitions are great transformations where terrestrial amniote clades returned to aquatic environments. These secondarily aquatic amniote clades include charismatic marine mammal and marine reptile groups, as well as countless semi-aquatic forms that modified their terrestrial locomotor anatomy to varying degrees to be suited for swimming via axial and/or appendicular propulsion. The terrestrial ancestors of secondarily aquatic groups would have started off swimming strikingly differently from one another given their evolutionary histories, as inferred by the way modern terrestrial amniotes swim. With such stark locomotor functional differences between reptiles and mammals, we ask if this impacted these transitions. Axial propulsion appears favored by aquatic descendants of terrestrially sprawling quadrupedal reptiles, with exceptions. Appendicular propulsion is more prevalent across the aquatic descendants of ancestrally parasagittal-postured mammals, particularly early transitioning forms. Ancestral terrestrial anatomical differences that precede secondarily aquatic invasions between mammals and reptiles, as well as the distribution of axial and appendicular swimming in secondarily aquatic clades, may indicate that ancestral terrestrial locomotor anatomy played a role, potentially in both constraint and facilitation, in certain aquatic locomotion styles. This perspective of the land-to-sea transition can lead to new avenues of functional, biomechanical, and developmental study of secondarily aquatic transitions.

Quadrupedal water launch capability demonstrated in small Late Jurassic pterosaurs.

Pterosaurs thrived in and around water for 160 + million years but their take-off from water is poorly understood. A purportedly low floating position and forward centre of gravity barred pterosaurs from a bird-like bipedal running launch. Quadrupedal water launch similar to extant water-feeding birds and bats has been proposed for the largest pterosaurs, such as Anhanguera and Quetzalcoatlus. However, quadrupedal water launch has never been demonstrated in smaller pterosaurs, including those living around the Tethys Sea in the Late Jurassic Solnhofen Lagoon. Using Laser-Stimulated Fluorescence, we singled out aurorazhdarchid specimen MB.R.3531 that alone preserved specific soft tissues among more than a dozen well-preserved Solnhofen pterosaur specimens. These soft tissues pertain to primary propulsive contact surfaces needed for quadrupedal water launch (pedal webbing and soft tissues from an articulated forelimb) that permit robust calculations of its dynamic feasibility without the need to make assumptions about contact areas. A first-principles-based dynamics model of MB.R.3531 reveals that quadrupedal water launch was theoretically feasible and that webbed feet significantly impacted launch performance. Three key factors limiting water launch performance in all pterosaurs are identified, providing a foundation for understanding water launch evolution: available propulsive contact area, forelimb extension range and forelimb extension power about the shoulder.

Pterosaurs evolved a muscular wing-body junction providing multifaceted flight performance benefits: Advanced aerodynamic smoothing, sophisticated wing root control, and wing force generation.

Pterosaurs were the first vertebrate flyers and lived for over 160 million years. However, aspects of their flight anatomy and flight performance remain unclear. Using laser-stimulated fluorescence, we observed direct soft tissue evidence of a wing root fairing in a pterosaur, a feature that smooths out the wing-body junction, reducing associated drag, as in modern aircraft and flying animals. Unlike bats and birds, the pterosaur wing root fairing was unique in being primarily made of muscle rather than fur or feathers. As a muscular feature, pterosaurs appear to have used their fairing to access further flight performance benefits through sophisticated control of their wing root and contributions to wing elevation and/or anterior wing motion during the flight stroke. This study underscores the value of using new instrumentation to fill knowledge gaps in pterosaur flight anatomy and evolution.

Response to Serrano and Chiappe.

In the recent study in Current Biology by Pei and colleagues1, we used two proxies - wing loading and specific lift - to reconstruct powered flight potential across the vaned feathered fossil pennaraptorans. The results recovered multiple origins of powered flight. We respectfully disagree with the criticism raised by Serrano and Chiappe2 that wing loading and specific lift, used in sequence, fail to discriminate between powered flight and gliding. We will explain this in reference to our original conservative approach.

Aerodynamics Show Membrane-Winged Theropods Were a Poor Gliding Dead-end.

The bizarre scansoriopterygid theropods Yi and Ambopteryx had skin stretched between elongate fingers that form a potential membranous wing. This wing is thought to have been used in aerial locomotion, but this has never been tested. Using laser-stimulated fluorescence imaging, we re-evaluate their anatomy and perform aerodynamic calculations covering flight potential, other wing-based behaviors, and gliding capabilities. We find that Yi and Ambopteryx were likely arboreal, highly unlikely to have any form of powered flight, and had significant deficiencies in flapping-based locomotion and limited gliding abilities. Our results show that Scansoriopterygidae are not models for the early evolution of bird flight, and their structurally distinct wings differed greatly from contemporaneous paravians, supporting multiple independent origins of flight. We propose that Scansoriopterygidae represents a unique but failed flight architecture of non-avialan theropods and that the evolutionary race to capture vertebrate aerial morphospace in the Middle to Late Jurassic was dynamic and complex.

Potential for Powered Flight Neared by Most Close Avialan Relatives, but Few Crossed Its Thresholds.

Uncertainties in the phylogeny of birds (Avialae) and their closest relatives have impeded deeper understanding of early theropod flight. To help address this, we produced an updated evolutionary hypothesis through an automated analysis of the Theropod Working Group (TWiG) coelurosaurian phylogenetic data matrix. Our larger, more resolved, and better-evaluated TWiG-based hypothesis supports the grouping of dromaeosaurids + troodontids (Deinonychosauria) as the sister taxon to birds (Paraves) and the recovery of Anchiornithinae as the earliest diverging birds. Although the phylogeny will continue developing, our current results provide a pertinent opportunity to evaluate what we know about early theropod flight. With our results and available data for vaned feathered pennaraptorans, we estimate the potential for powered flight among early birds and their closest relatives. We did this by using an ancestral state reconstruction analysis calculating maximum and minimum estimates of two proxies of powered flight potential-wing loading and specific lift. These results confirm powered flight potential in early birds but its rarity among the ancestors of the closest avialan relatives (select unenlagiine and microraptorine dromaeosaurids). For the first time, we find a broad range of these ancestors neared the wing loading and specific lift thresholds indicative of powered flight potential. This suggests there was greater experimentation with wing-assisted locomotion before theropod flight evolved than previously appreciated. This study adds invaluable support for multiple origins of powered flight potential in theropods (≥3 times), which we now know was from ancestors already nearing associated thresholds, and provides a framework for its further study. VIDEO ABSTRACT.

Volant Fossil Vertebrates: Potential for Bioinspired Flight Technology.

Animal flight is ecologically important and has a long evolutionary history. It has evolved independently in many distantly related clades of animals. Powered flight has evolved only three times in vertebrates, making it evolutionarily rare. Major recent fossil discoveries have provided key data on fossil flying vertebrates and critical insights regarding the evolution and different arrangements of animal flight surfaces. Combined with new methodologies, these discoveries have paved the way for potentially expanding biomimetic and biologically inspired designs to incorporate lessons from fossil taxa. Here, we review the latest knowledge and literature regarding flight performance in fossil vertebrates. We then synthesise key elements to provide an overview of those cases where fossil flyers might provide new insights for applied sciences.

The fast and the frugal: Divergent locomotory strategies drive limb lengthening in theropod dinosaurs.

Limb length, cursoriality and speed have long been areas of significant interest in theropod paleobiology, since locomotory capacity, especially running ability, is critical in the pursuit of prey and to avoid becoming prey. The impact of allometry on running ability, and the limiting effect of large body size, are aspects that are traditionally overlooked. Since several different non-avian theropod lineages have each independently evolved body sizes greater than any known terrestrial carnivorous mammal, ~1000kg or more, the effect that such large mass has on movement ability and energetics is an area with significant implications for Mesozoic paleoecology. Here, using expansive datasets that incorporate several different metrics to estimate body size, limb length and running speed, we calculate the effects of allometry on running ability. We test traditional metrics used to evaluate cursoriality in non-avian theropods such as distal limb length, relative hindlimb length, and compare the energetic cost savings of relative hindlimb elongation between members of the Tyrannosauridae and more basal megacarnivores such as Allosauroidea or Ceratosauridae. We find that once the limiting effects of body size increase is incorporated there is no significant correlation to top speed between any of the commonly used metrics, including the newly suggested distal limb index (Tibia + Metatarsus/ Femur length). The data also shows a significant split between large and small bodied theropods in terms of maximizing running potential suggesting two distinct strategies for promoting limb elongation based on the organisms' size. For small and medium sized theropods increased leg length seems to correlate with a desire to increase top speed while amongst larger taxa it corresponds more closely to energetic efficiency and reducing foraging costs. We also find, using 3D volumetric mass estimates, that the Tyrannosauridae show significant cost of transport savings compared to more basal clades, indicating reduced energy expenditures during foraging and likely reduced need for hunting forays. This suggests that amongst theropods, hindlimb evolution was not dictated by one particular strategy. Amongst smaller bodied taxa the competing pressures of being both a predator and a prey item dominant while larger ones, freed from predation pressure, seek to maximize foraging ability. We also discuss the implications both for interactions amongst specific clades and Mesozoic paleobiology and paleoecological reconstructions as a whole.

New perspectives on the origins of the unique vocal tract of birds.

Birds utilize a unique structure, called a syrinx, for the production of their vocalizations. The origins of the syrinx are not well understood. New work, utilizing first principles-based models, suggests that a key element in selection for the early syrinx might be the position of this vocal structure: although the larynx sits at the cranial end of the airway, the avian syrinx is located at the base of the airway at the split of the trachea to the lungs. This position may make the syrinx intrinsically more efficient, which might have been critical in the origin of this anatomical feature.

Evidence for the Cretaceous shark Cretoxyrhina mantelli feeding on the pterosaur Pteranodon from the Niobrara Formation.

A cervical vertebra of the large, pelagic pterodactyloid pterosaur Pteranodon sp. from the Late Cretaceous Niobrara Formation of Kansas, USA is significant for its association with a tooth from the large lamniform shark, Cretoxyrhina mantelli. Though the tooth does not pierce the vertebral periosteum, the intimate association of the fossils-in which the tooth is wedged below the left prezygapophysis-suggests their preservation together was not mere chance, and the specimen is evidence of Cretoxyrhina biting Pteranodon. It is not possible to infer whether the bite reflects predatory or scavenging behaviour from the preserved material. There are several records of Pteranodon having been consumed by other fish, including other sharks (specifically, the anacoracid Squalicorax kaupi), and multiple records of Cretoxyrhina biting other vertebrates of the Western Interior Seaway, but until now interactions between Cretoxyrhina and Pteranodon have remained elusive. The specimen increases the known interactions between large, pelagic, vertebrate carnivores of the Western Interior Seaway of North America during the Late Cretaceous, in addition to bolstering the relatively small fossil record representing pterosaurian interactions with other species.

The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents.

BACKGROUND: Powered flight is implicated as a major driver for the success of birds. Here we examine the effectiveness of three hypothesized pathways for the evolution of the flight stroke, the forelimb motion that powers aerial locomotion, in a terrestrial setting across a range of stem and basal avians: flap running, Wing Assisted Incline Running (WAIR), and wing-assisted leaping. METHODS: Using biomechanical mathematical models based on known aerodynamic principals and in vivo experiments and ground truthed using extant avians we seek to test if an incipient flight stroke may have contributed sufficient force to permit flap running, WAIR, or leaping takeoff along the phylogenetic lineage from Coelurosauria to birds. RESULTS: None of these behaviours were found to meet the biomechanical threshold requirements before Paraves. Neither was there a continuous trend of refinement for any of these biomechanical performances across phylogeny nor a signal of universal applicability near the origin of birds. None of these flap-based locomotory models appear to have been a major influence on pre-flight character acquisition such as pennaceous feathers, suggesting non-locomotory behaviours, and less stringent locomotory behaviours such as balancing and braking, played a role in the evolution of the maniraptoran wing and nascent flight stroke. We find no support for widespread prevalence of WAIR in non-avian theropods, but can't reject its presence in large winged, small-bodied taxa like Microraptor and Archaeopteryx. DISCUSSION: Using our first principles approach we find that "near flight" locomotor behaviors are most sensitive to wing area, and that non-locomotory related selection regimes likely expanded wing area well before WAIR and other such behaviors were possible in derived avians. These results suggest that investigations of the drivers for wing expansion and feather elongation in theropods need not be intrinsically linked to locomotory adaptations, and this separation is critical for our understanding of the origin of powered flight and avian evolution.

The locomotion of Babakotia radofilai inferred from epiphyseal and diaphyseal morphology of the humerus and femur.

Palaeopropithecids, or "sloth lemurs," are a diverse clade of large-bodied Malagasy subfossil primates characterized by their inferred suspensory positional behavior. The most recently discovered genus of the palaeopropithecids is Babakotia, and it has been described as more arboreal than Mesopropithecus, but less than Palaeopropithecus. In this article, the within-bone and between-bones articular and cross-sectional diaphyseal proportions of the humerus and femur of Babakotia were compared to extant lemurs, Mesopropithecus and Palaeopropithecus in order to further understand its arboreal adaptations. Additionally, a sample of apes and sloths (Choloepus and Bradypus) are included as functional outgroups composed of suspensory adapted primates and non-primates. Results show that Babakotia and Mesopropithecus both have high humeral/femoral shaft strength proportions, similar to extant great apes and sloths and indicative of forelimb suspensory behavior, with Babakotia more extreme in this regard. All three subfossil taxa have relatively large femoral heads, also associated with suspension in modern taxa. However, Babakotia and Mesopropithecus (but not Palaeopropithecus) have relatively small femoral head surface area to shaft strength proportions suggesting that hind-limb positioning in these taxa during climbing and other behaviors was different than in extant great apes, involving less mobility. Knee and humeral articular dimensions relative to shaft strengths are small in Babakotia and Mesopropithecus, similar to those found in modern sloths and divergent from those in extant great apes and lemurs, suggesting more sloth-like use of these joints during locomotion. Mesopropithecus and Babakotia are more similar to Choloepus in humerofemoral head and length proportions while Palaeopropithecus is more similar to Bradypus. These results provide further evidence of the suspensory adaptations of Babakotia and further highlight similarities to both extant suspensory primates and non-primate slow arboreal climbers and hangers. J. Morphol. 277:1199-1218, 2016. © 2016 Wiley Periodicals, Inc.

A specimen of Rhamphorhynchus with soft tissue preservation, stomach contents and a putative coprolite.

Despite being known for nearly two centuries, new specimens of the derived non-pterodactyloid pterosaur Rhamphorhynchus continue to be discovered and reveal new information about their anatomy and palaeobiology. Here we describe a specimen held in the collections of the Royal Tyrrell Museum of Palaeontology, Alberta, Canada that shows both preservation and impressions of soft tissues, and also preserves material interpreted as stomach contents of vertebrate remains and, uniquely, a putative coprolite. The specimen also preserves additional evidence for fibers in the uropatagium.

Fossil plotopterid seabirds from the Eo-Oligocene of the Olympic Peninsula (Washington State, USA): descriptions and functional morphology.

The plotopterids (Aves, Plotopteridae) were a group of extinct wing-propelled marine birds that are known from Paleogene-aged sediments (Eocene to Miocene), mostly around the Pacific Rim (especially Japan and the northwest coast of North America). While these birds exhibit a strikingly similar wing morphology to penguins (Spheniscidae), they also share derived characters with pelecaniform birds that are absent in penguins and exhibit apparently superficial similarities with auks (Alcidae: Charadriiformes). Despite quite an abundant fossil record, these birds have been little studied, and in particular their functional morphology remains little understood. Here we present osteological overviews of specimens from the northwest coast of Washington state (USA). We give an amended diagnosis for the well-represented North American genus, Tonsala Olson, 1980, describe a new large species, and examine the functional morphology of plotopterids showing that the ratio of humeral strength to femoral strength is quite low in one well-represented species Tonsala buchanani sp.nov., relative to both extant penguins and alcids. While the femoral strength of Tonsala buchanani is 'penguin-grade', its humeral strength is more 'alcid-grade'. These results have implications for understanding the mode-of-locomotion of these extinct marine birds. Although not related to Spheniscidae, our descriptions and functional results suggest that Tonsala buchanani sustained similar loads in walking, but slightly lower humeral loads during swimming, than a modern penguin. This suggests a swimming mode that is more similar to living alcids, than to the highly-specialised locomotor strategy of living and fossil penguins.

On the size and flight diversity of giant pterosaurs, the use of birds as pterosaur analogues and comments on pterosaur flightlessness.

The size and flight mechanics of giant pterosaurs have received considerable research interest for the last century but are confused by conflicting interpretations of pterosaur biology and flight capabilities. Avian biomechanical parameters have often been applied to pterosaurs in such research but, due to considerable differences in avian and pterosaur anatomy, have lead to systematic errors interpreting pterosaur flight mechanics. Such assumptions have lead to assertions that giant pterosaurs were extremely lightweight to facilitate flight or, if more realistic masses are assumed, were flightless. Reappraisal of the proportions, scaling and morphology of giant pterosaur fossils suggests that bird and pterosaur wing structure, gross anatomy and launch kinematics are too different to be considered mechanically interchangeable. Conclusions assuming such interchangeability--including those indicating that giant pterosaurs were flightless--are found to be based on inaccurate and poorly supported assumptions of structural scaling and launch kinematics. Pterosaur bone strength and flap-gliding performance demonstrate that giant pterosaur anatomy was capable of generating sufficient lift and thrust for powered flight as well as resisting flight loading stresses. The retention of flight characteristics across giant pterosaur skeletons and their considerable robustness compared to similarly-massed terrestrial animals suggest that giant pterosaurs were not flightless. Moreover, the term 'giant pterosaur' includes at least two radically different forms with very distinct palaeoecological signatures and, accordingly, all but the most basic sweeping conclusions about giant pterosaur flight should be treated with caution. Reappraisal of giant pterosaur material also reveals that the size of the largest pterosaurs, previously suggested to have wingspans up to 13 m and masses up to 544 kg, have been overestimated. Scaling of fragmentary giant pterosaur remains have been misled by distorted fossils or used inappropriate scaling techniques, indicating that 10-11 m wingspans and masses of 200-250 kg are the most reliable upper estimates of known pterosaur size.